Revista de la Sociedad Entomológica Argentina ISSN: 0373-5680 [email protected] Sociedad Entomológica Argentina Argentina

MARILUIS, Juan C.; SCHNACK, Juan A.; MULIERI, Pablo P.; PATITUCCI, Luciano D. (Diptera) from wild, suburban, and urban sites at three Southeast Patagonian localities Revista de la Sociedad Entomológica Argentina, vol. 67, núm. 1-2, 2008, pp. 107-114 Sociedad Entomológica Argentina Buenos Aires, Argentina

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Calliphoridae (Diptera) from wild, suburban, and urban sites at three Southeast Patagonian localities

MARILUIS, Juan C. */**, Juan A. SCHNACK */***, Pablo P. MULIERI, */** and Luciano D. PATITUCCI */**

* Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, Argentina. ** ANLIS «Dr. C. Malbrán», Departamento Vectores. Av. Vélez Sarsfield 563, 1281 Buenos Aires, Argentina; e-mail: [email protected], [email protected], [email protected], [email protected] *** División Entomología, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, Paseo del bosque s/nº, 1900 La Plata, Buenos Aires, Argentina; e- mail: [email protected]

Calliphoridae (Diptera) de ambientes no habitados, suburbanos y urbanos en tres localidades del sudeste patagónico

RESUMEN. Durante fines de la primavera-verano de 2004-2005, se analizó la composición, abundancia relativa y proporción de sexos de especies de Calliphoridae (Diptera) en las localidades de Caleta Olivia, Puerto Deseado y Puerto San Julián (Provincia de Santa Cruz, Argentina). Tres sitios de muestreo afectados diferencialmente por la intervención humana fueron seleccionados en cada localidad. En las áreas urbanas, las especies exóticas Calliphora vicina (Robineau-Desvoidy) y Phaenicia sericata (Meigen) fueron dominantes. Por el contrario, las nativas Compsomyiops fulvicrura (Robineau-Desvoidy) y Sarconesia chlorogaster (Wiedemann) predominaron tanto en áreas inhabitadas como en aquellas con bajo impacto humano. En los cebos utilizados para las capturas, se observó mayor proporción de hembras en todas las especies, excepto Sarconesia chlorogaster que mostró mayor proporción de machos.

PALABRAS CLAVE. Calliphoridae. Composición específica. Abundancia relativa. Sinantropía. Sudeste Patagonia.

ABSTRACT. Species composition, relative abundance, sex ratio and habitat preference of blowflies (Diptera: Calliphoridae) from Caleta Olivia, Puerto Deseado, and Puerto San Julián (Santa Cruz Province, Argentina) were studied during late spring and summer in 2004-2005. Results showed a higher prevalence of the exotic species, Calliphora vicina (Robineau-Desvoidy) and Phaenicia sericata (Meigen) at urban sites over the natives, Compsomyops fulvicrura (Robineau-Desvoidy) and Sarconesia chlorogaster (Wiedemann), which shows a strong preference for those sampling sites either not inhabited or less influenced by human activities. Sex ratio was female biased for all species, except for Sarconesia chlorogaster, which exhibited a male prevalence over females.

KEY WORDS. Calliphoridae. Species composition. Relative abundance. Synanthropy. Southeastern Patagonia.

Recibido: 27-IV-2007; aceptado: 29-II-2008 108 Rev. Soc. Entomol. Argent. 67 (1-2): 107-114, 2008

INTRODUCTION abundance and sex ratio, and the main factors governing them, considering sites differently Knowledge of the and ecology affected by human influence in three of blowfly species is important not only for localities along the Atlantic Patagonian coast. basic entomology, but also for other fields of science and its applications, especially sanitary biology. This is due to their role as MATERIAL AND METHODS pathogen vectors (Greenberg, 1971; Graczyk et al., 2001), indicators for forensic studies Study sites comprised urban (U), isolated (Byrd & Castner, 2001) and myiasis producers dwelling (ID) and wild (W) habitats at three (Zumpt, 1965; Hall & Wall, 1995). localities in northeastern Santa Cruz province: Many species are associated with Caleta Olivia (46º 26’ 17’’ S, 67º 32’ 05’’ W), environmental conditions created by man Puerto Deseado (47º 44’ 00’’ S, 65º 54’ 01’’ (synanthropy), especially muscoid (e.g., W), and Puerto San Julián (49º 17’ 60’’ S, Nuorteva, 1963). Habitat preferences of 67º 43’ 00’’ W). At each studied location, blowfly species and the structure of local the U sites were located in the geographical communities may exhibit significant center of the town, the ID sites were at the geographical variation (Nuorteva, 1963). city edge and the W sites were in the steppe, Comparative studies among wild, suburban, 5-8 km away from the urban limits. and urban environments housing calliphorid The study sites lie in the «Provincia species have been conducted in several Patagónica», where two main districts may geographic locations in Argentina, including be distinguished: the Central-Patagonian northeastern subtropics (Mariluis et al., 1990), (Puerto San Julián) and the San Jorge Gulf the suburbs of Buenos Aires city (Schnack et (Caleta Olivia and Puerto Deseado). The al., 1995), northwest (Mariluis & Schnack, former is mainly represented by a shrubby 1996) and mid-west Patagonia (Schnack et steppe dominated by Chuquiraga avellanedae al.,1998), southeastern Santa Cruz Province Lorentz (Asteraceae), Nassauvia glomerulosa and mid-eastern Tierra del Fuego (Schnack (Lag. Ex Pindl) and Stipa spp. (Poaceae); the & Mariluis, 2004). latter is dominated by Trevoa patagonica Speg According to findings from previous (Rhamnaceae) and Colliguaya integerrima works, similar values of specific composition Gill. et Hook. (Euphorbiaceae) (Cabrera, to the ones already registered in other 1971). localities of the Patagonian steppe are Blowflies are small and very mobile expected to be found. We hypothesize that organisms, which makes them difficult to differences in the species relative abundance sample at randomly-selected locations. Thus, among different sites, with variable degrees sampling methods are mostly based on of urbanization, will occur. We expect to find estimates or counts on aggregation sites, such a higher relative abundance of cosmopolitan as -attracting baits (Muirhead-Thomson, species among urban sectors of the coastal 1968). Samples were taken during the late localities of Patagonia, Argentina. spring and summer (November 2004- The use of carrion baits is crucial for the February 2005), once a month per site. Seven study of blowfly populations (Hall, 1995). The hourly captures of adult flies (10:00 am - majority of Calliphoridae females used them 04:00 pm) were taken with a hand net on a as protein sources for eggs maturation as well bait composed of 150 g of rotten cow meat as for egg-laying substrate (Erzinçlioglu, (five days old). The baits were exposed for 1996). Thus, we expect a bias toward females 15 minutes every hour. The sampling effort during capture. We will compare sex ratio in was the same at each site and consisted of order to quantitative describe how species one bait per site and seven netting events per will respond. date. Blowflies were killed in glass vials with The aim of this work was to analyze carbon tetrachloride and stored in the field blowfly species composition, relative as described elsewhere (Schnack & Mariluis, MARILUIS, J. C. et al. Calliphoridae from wild, suburban, and urban sites in Patagonia 109

1 a a a

0,5 b Prop. females

0 Cv Ps Cf Sch Species

Fig. 1. Proportion of females of blowfly species obtained from the nine capture sites (lowest and highest bars represent minimum and maximum values, respectively; middle bar refers to mean values). Data labeled with different letters are significantly different according to Dunn’s test (P < 0.05). Abbreviated names of species: Cv = Calliphora vicina; Ps = Phaenicia sericata; Cf = Compsomyiops fulvicrura; Sch = Sarconesia chlorogaster.

2004); once in the laboratory, they were using the non-parametric Mann-Whitney U identified and counted using the key of test for two independent samples (Zar, 1996). Mariluis & Schnack (2002). For this analysis, sites belonging to the same When calliphorid samplings are obtained habitat type were used as replicates. in several places at different dates, raw counts A correspondence analysis (CA) was used reflect the local sampling milieu at the to summarize the relationships between particular site and date, rather than any species and sites. This is a statistical fundamental differences among assemblages visualization method for illustrating the (McLeod & Donnelly, 1962). For this reason associations between the levels of a two-way our hypotheses are based on relative contingency table (Kent & Coker, 1992). For proportions. Raw data is given as this analysis raw number of flies gives complementary informative purpose. asymmetric scaling on the configuration of We took into account the proportion of species and sites. To avoid this potential effect males and females in order to describe the we give the same weight to all species. This response to the used bait. Thus, a Friedman’s was done by converting numbers collected analysis of variance by ranks was applied per site to percentage of the total yield per using the species as treatments and sites as species (total number of given species for all blocks, and Dunn’s procedure was performed sites) (Pollet, 2001). for multiple comparisons (Zar, 1996). Hypothesis of increasing proportions of exotic species with the urbanization, and the RESULTS opposite trend for the natives was assessed by the use of test for independent proportions A total of 2905 specimens were captured qualitatively ordered (Fleiss, 1981).These at the three surveyed localities; they included analyses were performed for each species at four species: the natives, Compsomyiops each locality. For this purpose we use fulvicrura (Robineau-Desvoidy) and numbers of flies of a given species over the Sarconesia chlorogaster (Wiedemann), and total number of flies per site. the exotics, Phaenicia sericata (Meigen) and The relative abundance of native species Calliphora vicina (Robineau-Desvoidy). among different habitats was compared by Males and females of the recorded species 110 Rev. Soc. Entomol. Argent. 67 (1-2): 107-114, 2008

Fig. 2. CA ordination diagram of sampling sites and localities (white squares) and calliphorid’s species (black dots) collected in Caleta Olivia (CO), Puerto Deseado (PD) and Puerto San Julián (PSJ). Site types, U: Urban, ID: Isolated Dwellings, W: Wild. Species abbreviations as in Fig. 1.

showed significant differences in their % of the data variability. According to the response to the bait used (ANOVA Chi first axis, the two native blowfly species recorded were located within the positive SquareN=7, df=3 = 13.29, P < 0.005). Due to female proportion, sex ratio was female right half of the diagram containing most of biased for Calliphora vicina (max-min range the W and ID sites, showing the ID site of values: 1.00–0.70), Phaenicia sericata (0.87– Caleta Olivia an intermediate position. On 0.72) and Compsomyiops fulvicrura (0.93– the other hand, the exotic species were 0.66). On the other hand, Sarconesia located on the left half. While Calliphora chlorogaster showed a male biased sex ratio vicina proportion was higher at U sites in according to its lower female proportion Puerto San Julian, Phaenicia sericata shows (0.67-0.13) (Fig. 1). the same trend in Caleta Olivia and Puerto The exotic, Phaenicia sericata and Deseado. On the other hand, axis two divides Calliphora vicina showed a higher proportion the urban sites in two major groups according of captures at the U sites in all studied to the occurrence of two dominant species. localities, being the former species The first one, Phaenicia sericata in Caleta significantly dominant. Their species relative Olivia and the second one, Calliphora vicina abundance decreased significantly towards in Puerto Deseado and San Julian. In the the W sites (Table I). On the contrary, the remaining habitats (sites ID and W) the native, Compsomyiops fulvicrura and homogeneity is influenced by Compsomyiops Sarconesia chlorogaster showed in most of fulvicrura (Fig. 2). the samples a high relative abundance in W From the ordination diagram, two main sites decreasing significantly in U sites (Table groups of sites can be considered according II). Nevertheless, this decrease from W to U to the relative abundance of two types of sites was not accounted for the few specimens blowflies: native and exotic species. The first of Sarconesia chlorogaster sampled at Caleta group included the six sites belonging to W Olivia. The CA ordination diagram shows this and ID habitats, while the second, all the trend with the arrangement of species and three U sites. Native species are significantly sites along the main axis (Fig. 2). The more abundant in ID-W sites (Mann-Whitney eigenvalues of axis 1 and 2 were 0.49 and P < 0.05) (Fig. 3). 0.05, respectively, the first expressing 83.32 MARILUIS, J. C. et al. Calliphoridae from wild, suburban, and urban sites in Patagonia 111

Fig. 3. Relative abundance of native blowflies in two groups of habitats: Urban (U) (n = 3) and Isolate Dwelling plus Wild Sites (ID-W) (n = 6). Columns represent median value and error bars represent first and third quartile. Columns labeled with different letters are significantly different (Mann-Whitney test P < 0.05).

Table I. Proportion and number of exotic calliphorid species, Calliphora vicina and Phaenicia sericata, obtained from each sampling site. P values account for differences among the proportions for the site types.

DISCUSSION the exotic species recorded may express the ecological disorder caused by urbanization, The higher prevalence of Phaenicia which usually favors the settlement of sericata and Calliphora vicina in U invasive species (Nuorteva, 1971; Schnack environments and that of Compsomyiops & Spinelli, 2000). fulvicrura and, secondarily of Sarconesia From a sanitary viewpoint, U sites chlorogaster, in W and ID sites in all studied provided useful information given that among localities suggest that native and exotic the recorded species, the dominant, species differ markedly in their habitat Phaenicia sericata and Calliphora vicina, selection. The high synanthropy displayed by show high sanitary importance. Phaenicia 112 Rev. Soc. Entomol. Argent. 67 (1-2): 107-114, 2008

Table II. Proportion and number of native calliphorid species, Compsomyiops fulvicrura and Sarconesia chlorogaster, obtained from each sampling site. P values account for differences among the proportions for the site types.

sericata, a nearly worldwide species, would scale instead of being at the species level be the most medically important blowfly. This (Schnack et al., 1998). endophylic and highly synanthropic species Female sex ratio was found for three is one of the primary myiasis producers in species. On the other hand, we cannot Europe, and to a lesser extent in Sudan, South explain why Sarconesia chlorogaster sampled Africa, and Australia (Baumgartner & from the baits used were male biased as it Greenberg, 1985). Moreover, cases of human was also observed in former studies (e.g., myiasis have been recorded in hospitals of Mariluis & Schnack, 1989; Mulieri et al., Chicago, Illinois, USA (Greenberg, 1984) and 2006). It would be possible that these species’ of Buenos Aires, Argentina (Mariluis & females are autogenic. Like most of blowfly Guarnera, 1983). Calliphora vicina exhibits species, if their eggs reached maturity without endophilic and communicative habits in the need of a protein meal, they would not urban settlements, and capacity to produce be compelled to feed on the bait. The myiasis on man and (Delhaes et al., attracting baits may indeed distort the actual 2001; Schnack & Mariluis, 2004). Even sex ratio, regardless of their nature. However, though, Calliphora vicina was not the most they do not necessarily alter species abundant species at U sites, it showed numerical trends. In a recent study carried preference for urban habitats. Nevertheless, out in the coastline of Buenos Aires city, during a survey carried out in Buenos Aires changes of blowfly species abundance outskirts (30º 35´ 28" S, 64º 12´ 22" W) displayed similar trends when captured either (Schnack et al., 1995) a synanthropic index on cow liver or on feces, being sex ratio (Nuorteva, 1963) calculated for this species female biased for most of the species, except was negative, suggesting its preference for the Sarconesia chlorogaster, whose females and wildness. On the other hand, this species was males were similarly represented (Mulieri et formerly regarded as synanthropic in Hungary al., 2006). (Mihalyí, 1967). Although these observations According to the data gathered in this seem contradictory, synanthropy may be an study, the low species richness of all study adequate approach at a local population sites is remarkable. This is in agreement to MARILUIS, J. C. et al. Calliphoridae from wild, suburban, and urban sites in Patagonia 113 former observations: blowfly species richness ACKNOWLEDGEMENTS shows a decrease as latitude increases as it was experienced in surveys previously We are grateful to Roberto Petrusic and undertaken in northeastern Argentina (14 Santiago Ansín for their valuable help in the species) (Mariluis et al., 1990), Buenos Aires field work. We appreciate the critical (12 species) (Schnack et al., 1995), and comments and constructive suggestions made western Patagonia (five species) (Mariluis & by Alejandro Farji-Brener, Diego Vázquez, Schnack, 1996) and eastern Patagonia (six and anonymous reviewers. This work was species) (Schnack & Mariluis, 2004). supported by a grant from the Technical and In a broad sense, species richness in the Scientific National Research Council of study sites was similar to the one recorded in Argentina (CONICET, PIP # 02008). formerly studied locations of Santa Cruz and Tierra del Fuego provinces (Schnack & Mariluis, 2004). Nevertheless, some LITERATURE CITED differences concerning species composition and relative abundance are worth being 1. BAUMGARTNER, D.L. & B. GREENBERG. 1985. Distribution and medical ecology of the blow flies highlighted if both surveys are compared. (Diptera: Calliphoridae) of Perú. Ann. Entomol. Soc. One of the main differences is the presence Am. 78: 565-587. 2. BYRD, J. H. & J. L. CASTNER. 2001. Forensic entomology: of Protophormia terraenovae at higher The utility of in legal investigations. latitudes (Schnack & Mariluis, 2004; Mariluis CRPress, London. & Schnack, 2005), not recorded in this study. 3. CABRERA, A. L. 1971. 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